PEP-1-heat shock protein 27 protects from neuronal damage in cells and in a Parkinson's disease mouse model

FEBS Journal

Volumn 279, Issue 11, 2012, Pages 1929-1942

  Lee, Yeom Pyo ^a   Kim, Dae Won ^a   Kang, Hye Won ^a   Hwang, Jae Hyeok ^a   Jeong, Hoon Jae ^a   Sohn, Eun Jeong ^a   Kim, Mi Jin ^a   Ahn, Eun Hee ^a   Shin, Min Jea ^a   Kim, Duk Soo ^b   Kang, Tae Cheon ^a   Kwon, Oh Shin ^c   Cho, Sung Woo ^d   Park, Jinseu ^a   Eum, Won Sik ^a   Choi, Soo Young ^a  

^a Hallym University   (South Korea)

^b Soonchunhyang University   (South Korea)

^c Kyungpook National University   (South Korea)

^d University of Ulsan College of Medicine   (South Korea)

Author keywords

Parkinson's disease; PEP 1 HSP27; protein therapy; protein transduction; ROS

Indexed keywords

PEP 1 HEAT SHOCK PROTEIN 27; PEPTIDE DERIVATIVE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA FRAGMENTATION; DOPAMINERGIC NERVE CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NERVE CELL LESION; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; 1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; CELL DEATH; CELL LINE, TUMOR; CYSTEAMINE; DNA FRAGMENTATION; DOPAMINERGIC NEURONS; ESCHERICHIA COLI; HSP27 HEAT-SHOCK PROTEINS; HUMANS; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PARKINSON DISEASE, SECONDARY; PEPTIDES; REACTIVE OXYGEN SPECIES; RECOMBINANT FUSION PROTEINS; ROTAROD PERFORMANCE TEST; SUBSTANTIA NIGRA;

EID: 84861199063     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08574.x     Document Type: Article

References (54)

1. Dawson TM, &, Dawson VL, (2003) Molecular pathways of neurodegeneration in Parkinson's disease. Science 302, 819-822. (Pubitemid 37339614)
2. Eriksen JL, Wszolek Z, &, Petrucelli L, (2005) Molecular pathogenesis of Parkinson disease. Arch Neurol 62, 353-357. (Pubitemid 40349469)
3. Janko J, &, Tolosa E, (1998) Parkinson's Disease and Movement Disorders, 3rd edn. Lippincott, Williams & Wilkins, New York, pp. 67-103.
4. Damier P, Hirsch EC, Agid Y, &, Graybiel AM, (1999) The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's diseases? Brain 122, 1437-1448. (Pubitemid 29374122)
5. Morales-Garcia JA, Redondo M, Alonso-Gil S, Gil C, Perex C, Martinez A, Santos A, &, Perez-Castillo A, (2011) Phosphodiesterase 7 inhibition preserves dopaminergic neurons in cellular and rodent models of Parkinson disease. PLoS One 6, e17240.
6. Dauer W, &, Przedborski S, (2003) Parkinson's disease: mechanisms and models. Neuron 39, 889-909. (Pubitemid 37130207)
7. Honot S, &, Hirsch EC, (2003) Neuroinflammatory processes in Parkinson's disease. Ann Neurol 53, S49-S60. (Pubitemid 36368562)
8. Warner TT, &, Schapira AH, (2003) Genetic and environmental factors in the cause of Parkinson's disease. Ann Neurol 53, S16-S25. (Pubitemid 36368559)
9. Eriksen JL, Przedborski S, &, Petrucelli L, (2005) Gene dosage and pathogenesis of Parkinson's disease. Trends Mol Med 11, 91-96. (Pubitemid 40348985)
10. +. Brain Res 1383, 99-107.
11. Chung YC, Ko HW, Bok E, Park ES, Huh SH, Nam JH, &, Jin BK, (2010) The role of neuroinflammation on the pathogenesis of Parkinson's disease. BMB Rep 43, 225-232.
12. Tasaki Y, Omura T, Yamada T, Ohkubo T, Suno M, Iida S, Sakaguchi T, Asari M, Shimizu K, &, Matsubara K, (2010) Meloxicam protects cell damage from 1-methyl-4-phenyl pyridinium toxicity via the phosphatidylinositol 3-kinase/Akt pathway in human dopaminergic neuroblastoma SH-SY5Y cells. Brain Res 1344, 25-33.
13. Yenari MA, Giffard RG, Sapolsky RM, &, Steinberg GK, (1999) The neuroprotective potential of heat shock protein 70 (HSP70). Mol Med Today 5, 525-531.
14. Hishiya A, &, Takayama S, (2008) Molecular chaperones as regulators of cell death. Oncogene 27, 6489-6506.
15. Tutar L, &, Tutar Y, (2010) Heat shock proteins: an overview. Curr Pharm Biotechnol 11, 216-222.
16. Kitamura Y, &, Nomura Y, (2003) Stress proteins and glial functions: possible therapeutic targets for neurodegenerative disorders. Pharmacol Ther 97, 35-53. (Pubitemid 35477803)
17. Slavotinek AM, &, Biesecker LG, (2001) Unfolding the role of chaperones and chaperonins in human disease. Trends Genet 17, 528-535. (Pubitemid 32763051)
18. Takayama S, Reed JC, &, Homma S, (2003) Heat-shock proteins as regulators of apoptosis. Oncogene 22, 9041-9047. (Pubitemid 38121704)
19. Latchman DS, (2005) HSP27 and cell survival in neurons. Int J Hyperthermia 21, 393-402.
20. Akbar MT, Wells DJ, Latchman DS, &, de Belleroche J, (2001) Heat shock protein 27 shows a distinctive widespread spatial and temporal pattern of induction in CNS glial and neuronal cells compared to heat shock protein 70 and caspase 3 following kainite administration. Mol Brain Res 93, 148-163. (Pubitemid 32925175)
21. Mailhos C, Howard MK, &, Latchman DS, (1993) Heat shock protects neuronal cells from programmed cell death by apoptosis. Neuroscience 55, 621-627. (Pubitemid 23226108)
22. Wagstaff MJ, Collaco-Moraes Y, Smith J, de Belleroche JS, Coffin RS, &, Latchman DS, (1999) Protection of neuronal cells from apoptosis by Hsp27 delivered with a herpes simplex virus-based vector. J Biol Chem 274, 5061-5069.
23. Almeida-Souza L, Goethals S, de Winter V, Dierick I, Gallardo R, Durme JV, Irobi J, Gettemans J, Rousseau F, Schymkowitz J, et al. (2010) Increased monomerization of mutants HSPB1 leads to protein hyperactivity in Charcot-Marie-Tooth neuropathy. J Biol Chem 285, 12778-12786.
24. Williams KL, &, Mearow KM, (2011) Phosphorylation status of heat shock protein 27 influences neurite growth in adult dorsal root ganglion sensory neurons in vitro. J Neurosci Res 89, 1160-1172.
25. Pasupuleti N, Gangadhariah M, Padmanabha S, Santhoshkumar P, &, Nagaraj RH, (2010) The role of the cysteine residue in the chaperone and anti-apoptotic functions of human Hsp27. J Cell Biochem 110, 408-419.
26. Bezard E, &, Przedborski S, (2011) A tale on animal models of Parkinson's disease. Mov Disord 26, 993-1002.
27. George S, Mok SS, Nurjono M, Ayton S, Finkelstein DI, Masters CL, Li QX, &, Culvenor JG, (2010) α-Synuclein transgenic mice reveal compensatory increase in Parkinson's disease-associated proteins DJ-1 and Parkin and have enhanced α-synuclein and PINK1 levels after rotenone treatment. J Mol Neurosci 42, 243-254.
28. St Martin JL, Klucken J, Outeiro TF, Nguyen P, Keller-McGandy C, Cantuti-Castelvetri I, Grammatopoulos TN, Standaert DG, Hyman BT, &, McLean PJ, (2007) Dopaminergic neuron loss and up-regulation of chaperone protein mRNA induced by targeted over-expression of alpha-synuclein in mouse substantia nigra. J Neurochem 100, 1449-1457. (Pubitemid 46376202)
29. Decamp E, &, Schneider JS, (2004) Attention and executive function deficits in chronic low-dose MPTP-treated non-human primates. Eur J Neurosci 20, 1371-1378. (Pubitemid 39233588)
30. + and paraquat neurotoxicity. Brain Res Bull 67, 509-514. (Pubitemid 41416747)
31. Nagel F, Falkenburger BH, Tonges L, Kowsky S, Poppelmeyer C, Schulz JB, Bahr M, &, Dietz GP, (2008) Tat-Hsp70 protects dopaminergic neurons in midbrain cultures and in the substantia nigra in models of Parkinson's disease. J Neurochem 105, 853-864. (Pubitemid 351562740)
32. Wadia JS, &, Dowdy SF, (2002) Protein transduction technology. Curr Opin Biotechnol 13, 52-56. (Pubitemid 34146548)
33. Morris MC, Depollier J, Mery J, Heitz F, &, Divita G, (2001) A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat Biotechnol 19, 1173-1176. (Pubitemid 33115705)
34. Eum WS, Kim DW, Hwang IK, Yoo KY, Kang TC, Jang SH, Choi HS, Choi SH, Kim YH, Kim SY, et al. (2004) In vivo protein transduction: biologically active intact PEP-1-superoxide dismutase fusion protein efficiently protects against ischemic insult. Free Radic Biol Med 37, 1656-1669.
35. Choi HS, An JJ, Kim SY, Lee SH, Kim DW, Yoo KY, Won MH, Kang TC, Kwon HJ, Kang JH, et al. (2006) PEP-1-SOD fusion protein efficiently protects against paraquat-induced dopaminergic neuron damage in a Parkinson disease mouse model. Free Radic Biol Med 41, 1058-1068. (Pubitemid 44331570)
36. Kim DW, Lee SH, Jeong MS, Sohn EJ, Kim MJ, Jeong HJ, An JJ, Jang SH, Won MH, Hwang IK, et al. (2010) Transduced Tat-SAG fusion protein protects against oxidative stress and brain ischemic insult. Free Radic Biol Med 48, 969-977.
37. Ahn EH, Kim DW, Kang HW, Shin MJ, Won MH, Kim J, Kim DJ, Kwon OS, Kang TC, Han KH, et al. (2010) Transduced PEP-1-ribosomal protein S3 (rpS3) ameliorates 12-O-tetradecanoylphorbol-13-acetate-induced inflammation in mice. Toxicol 276, 192-197.
38. An JJ, Lee YP, Kim SY, Lee SH, Lee MJ, Jeong MS, Kim DW, Jang SH, Yoo KY, Won MH, et al. (2008) Transduced human PEP-1-heat shock protein 27 efficiently protects against brain ischemic insult. FEBS J 275, 1296-1308. (Pubitemid 351342224)
39. Kim MJ, Kim DW, Yoo KY, Sohn EJ, Jeong HJ, Kang HW, Shin MJ, Ahn JJ, Kwon SW, Kim YN, et al. (2010) Protective effects of transduced PEP-1-Frataxin protein on oxidative stress-induced neuronal cell death. J Neurol Sci 298, 64-69.
40. Kim SY, Kim MY, Mo JS, Park JW, &, Park HS, (2007) SAG protects human neuroblastoma SH-SY5Y cells against 1-methyl-4-phenylpyridinium ion (MPP+)-induced cytotoxicity via the downregulation of ROS generation and JNK signaling. Neurosci Lett 413, 132-136.
41. Dietz GP, (2010) Cell-penetrating peptide technology to delivery chaperones and associated factors in diseases and basic research. Curr Pharm Biotechnol 11, 167-174.
42. Lim KS, Won YW, Park YS, &, Kim YH, (2010) Preparation and functional analysis of recombinant protein transduction domain-metallothionein fusion proteins. Biochimie 92, 964-970.
43. Wang H, Zhong CY, Wu JF, Huang YB, &, Liu CB, (2010) Enhancement of TAT cell membrane penetration efficiency by dimethyl sulphoxide. J Control Release 143, 64-70.
44. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, &, Lebleu B, (2003) Cell-permeable peptides: a reevaluation of the mechanism of cellular uptake. J Biol Chem 278, 585-590. (Pubitemid 36043612)
45. Lee MJ, Kim DW, Sohn EJ, Jeong HJ, Shin MJ, Kang HW, Ahn EH, Kwon SW, Kim YN, Won MH, et al. (2011) Anti-inflammatory effect of transduced PEP-1-cyclophilin A in Raw 264.7 cells and 12-O-tetradecanoylphobol-13-acetate- induced mice. Life Sci 89, 896-904.
46. Halliwell B, &, Gutteridge JMC, (1999) Free Radicals in Biology and Medicine. Oxford University Press, Oxford.
47. Hald A, &, Lotharius J, (2005) Oxidative stress and inflammation in Parkinson's disease: is there a causal link? Exp Neurol 193, 279-290. (Pubitemid 40616179)
48. Jackson-Lewis V, &, Przedborski S, (2007) Protocol for the MPTP mouse model of Parkinson's disease. Nat Protoc 2, 141-151. (Pubitemid 47044700)
49. Thiruchelvam M, Prokopenko O, Cory-Slechta DA, Richfield EK, Buckley B, &, Mirochnitchenko O, (2005) Overexpression of superoxide dismutase or glutathione peroxide protects against the paraquat+mabeb-induced Parkinson disease phenotype. J Biol Chem 280, 22530-22539. (Pubitemid 40827911)
50. Bradford M, (1976) A rapid and sensitive method for the quantitation of microgram quantities utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
51. Nare B, Allocco JJ, Kuningas R, Galuska S, Myers RW, Bennarek MA, &, Schmatz DM, (1999) Development of a scintillation proximity assay for histone deacetylase using a biotinylated peptide derived from histone-H4. Anal Biochem 267, 390-396. (Pubitemid 29095888)
52. Park J, Ryu J, Kim KA, Lee HJ, Bahn JH, Han K, Choi EY, Lee KS, Kwon HY, &, Choi SY, (2002) Mutational analysis of a human immunodeficiency virus type 1 Tat protein transduction domain which is required for delivery of an exogenous protein into mammalian cells. J Gen Virol 83, 1173-1181. (Pubitemid 34477291)
53. Manning-Bog AB, McCormack AL, Pufisai MG, Bolin LM, &, Di Monte DA, (2003) α-Synuclein overexpression protects against paraquat-induced neurodegeneration. J Neurosci 23, 3095-3099. (Pubitemid 36531948)
54. Iwamoto T, Okumura S, Iwatsubo K, Kawabe JI, Ohtsu K, Sakai I, Hashimoto Y, Izumitani A, Sango K, Ajiki K, et al. (2003) Motor dysfunction in type 5 adenylyl cyclase-null mice. J Biol Chem 278, 16936-16940. (Pubitemid 36799567)